Choroidal microvascular dropout as a biomarker of glaucoma progression in patients with diabetes mellitus

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PURPOSE

To study the occurrence, features of the development of choroidal microvascular dropout (CMvD) as a possible marker of the severity of the glaucoma process and to assess the impact of diabetes mellitus (DM) on the progression of these changes.

MATERIAL AND METHODS

The study included 258 eyes (258 patients), which were divided into groups: 1st — 58 patients (58 eyes) with stage I POAG and DM; 2nd — 50 patients (50 eyes) with stage I POAG; 3rd — 50 patients (50 eyes) with stage III POAG and DM; 4th — 50 patients (50 eyes) with stage III POAG; 5th — 50 patients (50 eyes) with DM. The observation period lasted 24 months. The occurrence and dynamics of the development of CMvD, their relationship with structural and functional indicators of the optic disc in the course of observation were evaluated in patients with POAG and DM.

RESULTS

CMvD was detected in stage I POAG in 17 eyes (34%), in patients with DM — in 27 eyes (54%), in the combined course of stage I POAG and DM — in 46 eyes (79.31%), in patients with stage III glaucoma — in 100% of cases. In patients with stage III glaucoma, the CMvD area indicators exceeded the values in other groups and practically did not differ regardless the presence of DM (0.59±0.13 mm², p=0.005) and its absence (0.57±0.14 mm², p=0.005). In the first year of follow-up, the increase in the area size of microvascular disorders in patients with POAG I was 5.88%, in comorbid patients — 3.84%, but by the end of the follow-up it increased by 19.23%, and in the group of patients with a high rate of progression — by 31.25%. Strong reliable correlations of CMvD with mean deviation (r=0.89) were revealed, as well as moderate correlations — with structural indicators of the optic disc (r=0.59) and with hemodynamic indicators (r=0.54 and r=0.52).

CONCLUSION

Development of CMvD is both a result of glaucomatous damage to the optic nerve and a consequence of a disruption of its hemodynamics at the level of the deep capillary plexus. The results of the study demonstrate the adverse effect of DM on the course of glaucoma, which determines the initiation of microvascular disorders that aggravate the severity of the glaucoma process and the rate of its progression.

Keywords:

OCT angiography

choroidal microvascular dropout

vascular density

perfusion density

primary open-angle glaucoma

diabetes mellitus

Authors:

Fursova A.Zh.

Novosibirsk State Regional Clinical Hospital;
Novosibirsk State Medical University

Gamza Yu.A.

Novosibirsk State Medical University;
Private Healthcare institution Clinical Hospital «RZD-Medicine» Novosibirsk

Derbeneva A.S.

Novosibirsk State Regional Clinical Hospital;
Novosibirsk State Medical University

Vasilyeva M.A.

Novosibirsk State Regional Clinical Hospital

Tarasov M.S.

Novosibirsk State Regional Clinical Hospital;
Novosibirsk State Medical University

Zubkova M.Y.

Novosibirsk State Regional Clinical Hospital;
Novosibirsk State Medical University

Received:

11.07.2022

Accepted:

29.08.2022

List of references:

Kurysheva NI. The role of retinal microcirculation disorders in the progression of glaucomatous optic neuropathy. The Russian Annals of Ophthalmology = Vestnik oftal’mologii. 2020;136(4):57-65. (In Russ.). https://doi.org/10.17116/oftalma202013604157
Kurysheva NI, Maslova EV, Zolnikova IV, Fomin AV, Lagutin MB. A comparative study of structural, functional and circulatory parameters in glaucoma diagnostics. PLoS ONE. 2018;13(8):e0201599. https://doi.org/10.1371/journal.pone.0201599
Roberts KF, Artes PH, O’Leary N, et al. Peripapillary choroidal thickness in healthy controls and patients with focal, diffuse, and sclerotic glaucomatous optic disc damage. Arch Ophthalmol. 2012;130(8):980-986. https://doi.org/10.1001/archophthalmol.2012.371
Fursova AZh, Gamza YuA, Tarasov MS, Vasil’eva MA, Derbeneva AS. A comparative study of structural and microcirculatory parameters in patients with primary open-angle glaucoma and diabetes mellitus. Russian Ophthalmological Journal = Rossiyskiy oftal’mologicheskiy zhurnal. 2020;13(3):42-50. (In Russ.). https://doi.org/10.21516/2072-0076-2020-13-3-42-50
Suh MH, Zangwill LM, Manalastas PI, Belghith A, Yarmohammadi A, Medeiros FA, Diniz-Filho A, Saunders LJ, Weinreb RN. Deep Retinal Layer Microvasculature Dropout Detected by the Optical Coherence Tomography Angiography in Glaucoma. Ophthalmology. 2016;123(12):2509-2518. https://doi.org/10.1016/j.ophtha.2016.09.002
Ichiyama Y, Minamikawa T, Niwa Y, Ohji M. Capillary Dropout at the Retinal Nerve Fiber Layer Defect in Glaucoma: An Optical Coherence Tomography Angiography Study. J Glaucoma. 2017;26(4):142-145. https://doi.org/10.1097/IJG.0000000000000540
Suh MH, Zangwill LM, Manalastas P, Belghith A, Yarmohammadi A, Akagi T, Diniz-Filho A, Saunders L, Weinreb RN. Deep-Layer Microvasculature Dropout by Optical Coherence Tomography Angiography and Microstructure of Parapapillary Atrophy. Invest Ophthalmol Vis Sci. 2018;59(5): 1995-2004. https://doi.org/10.1167/iovs.17-23046
Sung MS, Heo H, Park SW. Microstructure of Parapapillary Atrophy Is Associated With Parapapillary Microvasculature in Myopic Eyes. Am J Ophthalmol. 2018;192:157-168. https://doi.org/10.1016/j.ajo.2018.05.022
Kim JA, Lee EJ, Kim TW. Evaluation of parapapillary choroidal microvasculature dropout and progressive retinal nerve fiber layer thinning in patients with glaucoma. JAMA Ophthalmol. 2019;137(7):810-816. https://doi.org/10.1001/jamaophthalmol.2019.1212
Fursova AZh, Gamza YuA, Tarasov MS, Derbeneva AS. Primary open-angle glaucoma in patients with diabetes mellitus: pathogenetic and clinical parallels of development (literature review). National Journal Glaucoma = Natsional’nyy zhurnal Glaukoma. 2020;19(2):66-74. (In Russ.). https://doi.org/10.25700/NJG.2020.02.08
Fursova AZh, Gamza YuA, Gusarevich OG, Derbeneva AS, Vasil’eva MA. The changes of functional, structural and hemodynamic parameters of the optic disc in patients with primary open-angle glaucoma and diabetes mellitus in long-term follow-up. Russian Ophthalmological Journal = Rossiyskiy oftal’mologicheskiy zhurnal. 2021;14(3):54-64. (In Russ.). https://doi.org/10.21516/2072-0076-2021-14-3-54-64
Fursova AZh, Gamza YuA, Gusarevich OG, Derbeneva AS, Vasilyeva MA, Chubar NV, Tarasov MS. Analysis of changes in structural and hemodynamic parameters of the retina and foveolar avascular zone in patients with primary open-angle glaucoma and diabetes mellitus observed in long-term follow-up. National Journal Glaucoma = Natsional’nyi zhurnal Glaukoma. 2021;20(3):59-77. (In Russ.). https://doi.org/10.25700/2078-4104-2021-20-3-59-77
Kurysheva NI, Maslova EV, Trubilina AV, Fomin AV, Lagutin MB. Pattern electroretinogram and macular perfusion in glaucoma. The Russian Annals of Ophthalmology = Vestnik oftal’mologii. 2018;134(4):34-40. (In Russ.). https://doi.org/10.17116/oftalma201813404134
Petrachkov DV, Budzinskaya MV. Biomarkers of diabetic retinopathy on optical coherence tomography angiography. The Russian Annals of Ophthalmology = Vestnik oftal’mologii. 2020;136(4):344-353. (In Russ.). https://doi.org/10.17116/oftalma2020136042344
Jo YH, Shin JW, Song MK, Won HJ, Kook MS. Choroidal microvasculature dropout is associated with generalized choroidal vessel loss within the beta-parapapillary atrophy in glaucoma. Am J Ophthalmol. 2020;215:37-48. https://doi.org/10.1016/j.ajo.2020.03.009
Kwon J, Shin JW, Lee J, Kook MS. Choroidal microvasculature dropout is associated with parafoveal visual field defects in glaucoma. Am J Ophthalmol. 2018;188:141-154. https://doi.org/10.1016/j.ajo.2018.01.035
Lee EJ, Kim T-W, Lee SH, Kim J-A. Underlying microstructure of parapapillary deep-layer capillary dropout identified by optical coherence tomography angiography. Invest Ophthalmol Vis Sci. 2017;58:1621-1627. https://doi.org/10.1167/iovs.17-21440
Rao HL, Sreenivasaiah S, Riyazuddin M, Dasari S, et al. Choroidal Microvascular Dropout in Primary Angle Closure Glaucoma. Am J Ophthalmol. 2019;199:184-192. https://doi.org/10.1016/j.ajo.2018.11.021
Lee EJ, Kim J-A, Kim T-W. Influence of Choroidal Microvasculature Dropout on the Rate of Glaucomatous Progression: A Prospective Study. Ophthalmol Glaucoma. 2020;3(1):25-31. https://doi.org/10.1016/j.ogla.2019.10.001
Lee EJ, Kee HJ, Park KA, Han JC, Kee C. Comparative topographical analysis of choroidal microvascular dropout between glaucoma and nonarteritic anterior ischemic optic neuropathy. Invest Ophthalmol Vis Sci. 2021;62(13):27. https://doi.org/10.1167/iovs.62.13.27
Kim G-N, Lee EJ, Kim T-W. Parapapillary choroidal microvasculature dropout in nonglaucomatous healthy eyes. Acta Ophthalmol. 2020;98(6):754-760. https://doi.org/10.1111/aos.14385
Shin DY, Jeon SJ, Kim EK, Jung KI, Park HYL, Park CK. Association between peripapillary scleral deformation and choroidal microvascular circulation in glaucoma. Sci Rep. 2019;9(1):18503. https://doi.org/10.1038/s41598-019-54882-9
Toshev AP, Schuster AK, Ul Hassan SN, Pfeiffer N, Hoffmann EM. Optical Coherence Tomography Angiography of Optic Disc in Eyes With Primary Open-angle Glaucoma and Normal-tension Glaucoma. J Glaucoma. 2019;28(3):243-251. https://doi.org/10.1097/IJG.0000000000001184